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BE Manuscript Version for Press Title: Risk assessment and the use of novel shortcuts in spatial detouring tasks in jumping spiders Abbreviated title: Route assessment in jumping spiders Samuel Aguilar-Argüello¹; Daniel Gerhard²; Ximena J. Nelson¹* ¹School of Biological Sciences, University of Canterbury, Christchurch, New Zealand ²School of Mathematics and Statistic, University of Canterbury, Christchurch, New Zealand *Author for correspondence: [email protected] Address: School of Biological Sciences, University of Canterbury, Private Bag 4800, Christchurch, New Zealand. Phone: +6433695198 Abstract Selection on individuals that incorporate risk to quickly and accurately make a priori navigational assessments may lead to increased spatial ability. Jumping spiders (Araneae: Salticidae) are characterized by their highly acute vision, which mediates many behaviors, including prey capture and navigation. When moving to a specific goal (prey, nest, a potential mate, etc.), salticids rely on visual cues and spatial memory to orient in three-dimensional space. Salticid spatial ability has been studied in homing and detour tasks, with Portia being considered one of the most skillful genera in terms of spatial ability in the family. Commonly living in complex environments, salticids are likely to encounter a wide variety of routes that could lead to a goal, and, as selection favors individuals that can accurately make assessments, they may be able to assess alternative route distances to select the most efficient route. Here, we tested whether two salticid species (Portia fimbriata and Trite planiceps) can discriminate and assess between different available routes by their length, and riskiness to escape from a stressful scenario. Results suggest that while Portia is more likely to choose 1 the easiest and shortest escape routes, Trite is faster in both decision-making about which route to take, and to escape. However, some individuals were able to use novel shortcuts instead of the routes expected, with Portia containing a higher proportion of shortcut-takers than Trite. These differences in spatial ability seem to correspond with the environmental complexity inhabited by each species. Key Words: Cognition, salticid, decision-making, detour behavior, environmental complexity, route choice. 2 INTRODUCTION Assessment is the process by which animals evaluate perceived stimuli, converting them to an informational state to determine a specific level of risk or benefit (Blumstein and Bouskila 1996), while decision-making is a cognitive process that allows animals to evaluate their environment, so they can avoid less favorable situations. Thus, decision-making follows assessment and precedes observable behavior (Blumstein and Bouskila 1996). Because of increased ability to take the most efficient route to a goal, selection favors those individuals that can more quickly and accurately make assessments (Helfman 1989, Lima and Bednekoff 1999, Mirza and Chivers 2001, Brown 2003, Golub and Brown 2003). For example, in a food gathering task, selection of inefficient routes results in prolonged foraging, higher energetic cost, decreased time spent on other activities, and increased predation risk (Gibson et al. 2007). Efficient route use has been observed in bees that integrate information about flight path vectors (‘path integration’) to navigate to the colony or a food source (Cartwright and Collett 1983), allowing them to make novel shortcuts, even if they cannot see the goal (Dyer 1991, Menzel et al. 2005, 2011). Similarly, shortcuts have been observed in desert ants (Wehner and Wehner 1990) and wandering spiders (Seyfarth et al. 1982). In these cases, proprioceptive mechanisms are used, and the distance assessment of the alternative routes is only done after experience. Here, we investigate whether invertebrates with no previous experience can assess different routes beforehand and follow the most efficient route to reach a goal, without the use of path integration. Animals that pounce on their prey, such as jumping spiders (Salticidae), are ideal subjects to investigate decision-making. Salticids have a highly-developed visual system (Land et al. 2012) and perform precision jumps for predation and locomotion, accurately assessing the distance to the landing point (Nabawy et al. 2018). Furthermore, when a salticid identifies a prey, it is sometimes forced to take a detour, as the direct route is either inaccessible (Tarsitano and Jackson 1997), or disadvantageous (Jackson and Pollard 1996, Jackson and Wilcox 1993). Salticid detours are preceded by scanning behavior which is characterized by a systematic movement of the body in order to 3 visually inspect its surroundings (Tarsitano and Andrew 1999). Scanning is useful for visual inspection and route selection, but is also a crucial stage for navigation, as the individual potentially plans the route ahead of time (Cross and Jackson 2016). Previous detour-related tasks have shown that salticids can discriminate between routes that lead to a moving or non-moving prey item from routes that do not (Tarsitano and Jackson 1992, 1994, 1997; Tarsitano and Andrew 1999; Tarsitano 2006), but work to date has not considered risk assessment in detour tasks. Commonly living in complex environments, salticid ability to find the best route out of a vast number of alternative pathways could be crucial to save energy and time, and avoid predation. Therefore, salticids may be able to assess, beforehand, alternative routes to select the optimum route. While detouring is a spatial ability apparently widespread among the Salticidae, there is a particular genus that stands out due to its exceptional cognitive abilities and its behavioral flexibility (Jackson and Pollard 1996; Jackson and Cross 2011). Portia lives in complex rainforest habitats in which it preys upon spiders (Jackson and Wilcox 1990; Harland and Jackson 2000). To reach prey, Portia can perform complex detours spanning over a meter, while losing sight of its prey for more than 80 min (Jackson and Hallas 1986a; Jackson and Wilcox 1993). This suggests not only an outstanding sense of orientation in three-dimensional space, but also spatial memory due to the spider’s need to move out of line-of-sight of the prey to follow the detour. Here, our main objective was to determine if salticids can a priori assess route distance and riskiness, but our study differs from previous work in that there was no clear best goal (e.g., prey) which was reached by a single correct route; rather the goal itself was to choose the most efficient (or least risky) way out of a stressful situation. Our routes were also discontinuous, being made up of dowels, such that the problem may be conceived of as a series of sub-goals which needed to be connected in advance in order to achieve the least risky outcome (escape) which was, in itself, identical for all routes. We first tested if salticids differentiate the distance between the dowels and choose a route representing the safest option. Secondly, we tested whether they can discriminate between different routes according to length, and choose the most suitable one in order to escape a 4 stressful scenario. Additionally, we explored whether there are intraspecific and interspecific differences in route assessment. Being from a complex habitat (Jackson and Blest 1982), and known for its cognitive ability (Jackson and Pollard 1996; Jackson and Cross 2011), we predicted that Portia fimbriata would be more effective at making efficient route choices compared with a salticid from a less complex habitat and not known for exceptional cognitive ability, Trite planiceps. Our prediction is based on the clever foraging hypothesis, which postulates that individuals living in more complex environments have better neurobiological navigational abilities (Striedter 2005; Park and Bell 2010). As salticid performance improves with knowledge about the environment (Edwards and Jackson 1994; Aguilar-Arguello et. al 2018), we also predicted that adults would outperform subadults. Additionally, we predicted that females would outperform males, as they are typically the more motivated sex, at least in predation-based or learning tasks (Jackson and Wilcox 1990; Jackson and Pollard 1996; Jakob and Long 2016). METHODS Test animals and maintenance Experiments were carried out from 0800 to 1300 h in the laboratory at the University of Canterbury. Trite planiceps Simon is a large (6-13 mm) salticid endemic to New Zealand and is typically found in coastal areas where it inhabits the rolled-up flax leaves of Phormium tenux and Cordyline spp. (Forster 1979). T. planiceps were field-collected in Christchurch, and were transferred to the laboratory, where they were housed individually in 1 L transparent plastic containers. Individuals were held in captivity for at least one week before testing. Spiders were fed once a week with two adult Musca domestica. Water supply was available through a cotton wick submerged in water which protruded into the container. Portia fimbriata Doleschall is a large (6-11 mm) salticid from the rainforests of Northern Australia (Jackson and Hallas, 1986a). P. fimbriata were lab-reared and, being predominantly araneophagic (spider-eating), were fed a combination of Musca domestica and a Badumna longinqua 5 spider once a week. Individuals were housed as above. Test arena Salticid aversion to water is frequently used as a motivational tool in detour experiments (Cross and Jackson 2016). Here our aim was for spiders to choose a route to escape the stressful scenario of being surrounded by water by getting to the platform edge, rather than choosing a route to a specific target goal, such as prey. Our trials were performed in a 43 x 43 x 7 cm plastic container (pool) filled with water to a depth of 6 cm. From a central starting platform (PVC dowel, 9 cm high x 3.5 cm diameter) four possible escape routes extended to each of the four sides of the pool. Escape routes consisted of a series of PVC dowels (7 cm high x 1 cm diameter) protruding 1 cm from the water. These led to identical high-resolution pictures of foliage which surrounded the pool to both motivate the spiders to exit the pool and to provide visual obstruction of external visual stimuli.
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